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Ice Hockey Summit II: Zero Tolerance for Head Hits and Fighting

Smith, Aynsley M. RN, PhD1; Stuart, Michael J. MD1; Dodick, David W. MD2; Roberts, William O. MD, FACSM3; Alford, Patrick W. PhD4; Ashare, Alan B. MD5; Aubrey, Mark MD6; Benson, Brian W. MD, PhD7; Burke, Chip J. MD8; Dick, Randall MS, FACSM9; Eickhoff, Chad ATR, ATC1; Emery, Carolyn A. PhD7; Flashman, Laura A. PhD10; Gaz, Daniel V. MSc1; Giza, Chris C. MD11; Greenwald, Richard M. PhD12; Herring, Stanley A. MD, FACSM13; Hoshizaki, T. Blaine PhD14; Hudziak, James J. MD, PhD15; Huston, John III MD16; Krause, David PT, DSc1; LaVoi, Nicole PhD17; Leaf, Matt18; Leddy, John J. MD19; MacPherson, Alison PhD20; McKee, Ann C. MD21; Mihalik, Jason P. PhD22; Moessner, Anne M. RN, CNS23; Montelpare, William J. PhD24; Putukian, Margot MD, FACSM25; Schneider, Kathryn J. PhD26; Szalkowski, Ron27; Tabrum, Mark18; Whitehead, James R.28; Wiese-Bjornstal, Diane M. PhD29

doi: 10.1249/JSR.0000000000000132
Special Communications

This study aimed to present currently known basic science and on-ice influences of sport-related concussion (SRC) in hockey, building upon the Ice Hockey Summit I action plan (2011) to reduce SRC. The prior summit proceedings included an action plan intended to reduce SRC. As such, the proceedings from Summit I served as a point of departure for the science and discussion held during Summit II (Mayo Clinic, Rochester, MN, October 2013). Summit II focused on 1) Basic Science of Concussions in Ice Hockey: Taking Science Forward, 2) Acute and Chronic Concussion Care: Making a Difference, (3) Preventing Concussions via Behavior, Rules, Education, and Measuring Effectiveness, 4) Updates in Equipment: Their Relationship to Industry Standards, and 5) Policies and Plans at State, National, and Federal Levels To Reduce SRC. Action strategies derived from the presentations and discussion described in these sectors were voted on subsequently for purposes of prioritization. The following proceedings include the knowledge and research shared by invited faculty, many of whom are health care providers and clinical investigators. The Summit II evidence-based action plan emphasizes the rapidly evolving scientific content of hockey SRC. It includes the most highly prioritized strategies voted on for implementation to decrease concussion. The highest-priority action items identified from the Summit include the following: 1) eliminate head hits from all levels of ice hockey, 2) change body checking policies, and 3) eliminate fighting in all amateur and professional hockey.

1Sports Medicine Center, Mayo Clinic, Rochester, MN; 2Department of Neurology, Mayo Clinic, Scottsdale, AZ; 3Department of Family Medicine and Community Health, University of Minnesota- Twin Cities, Minneapolis, MN; 4Department of Biomedical Engineering, University of Minnesota-Twin Cities, Minneapolis, MN; 5Department of Radiology, St. Elizabeth’s Medical Center, Boston, MA; 6International Ice Hockey Federation and Hockey Canada and Ottawa Sport Medicine Centre, Ottawa, Ontario, Canada; 7Sport Medicine Centre, University of Calgary, Calgary, Alberta, Canada; 8Department of Orthopedics, University of Pittsburg Medical Center-St. Margaret, Pittsburg, PA; 9National Collegiate Athletic Association, Indianapolis, IN; 10Department of Psychiatry, Geisel School of Medicine at Dartmouth, Dartmouth College, Hanover, NH; 11Division of Pediatric Neurology, Mattel Children’s Hospital and David Geffen School of Medicine at UCLA, Los Angeles, CA; 12Simbex, LLC, Lebanon, NH; 13Department of Family Medicine, University of Washington, Seattle, Washington; 14School of Human Kinetics, University of Ottawa, Ottawa, Ontario, Canada; 15Department of Psychiatry, University of Vermont Medical Center, Burlington, VT; 16Department of Radiology, Mayo Clinic, Rochester, MN; 17School of Kinesiology, University of Minnesota-Twin Cities, Minneapolis, MN; 18USA Hockey, Colorado Springs, CO; 19Department of Orthopaedics, University of New York at Buffalo, Buffalo, NY; 20School of Kinesiology and Health Science, York University, Toronto, Ontario, Canada; 21Center for the Study of Traumatic Encephalopathy, Boston University School of Medicine, Boston, MA; 22Department of Exercise and Sport Science, The University of North Carolina, Chapel Hill, NC; 23Department of Nursing, Mayo Clinic, Rochester, MN; 24Department of Applied Human Sciences, University of Prince Edward Island, Charlottetown, Prince Edward Island, Canada; 25Department of Athletic Medicine, Princeton University, Princeton, New Jersey; 26Sport Injury Prevention Research Centre, University of Calgary, Calgary, Alberta, Canada; 27Team Wendy, Cleveland, OH; 28American College of Sports Medicine, Indianapolis, IN; and 29Department of Kinesiology, University of Minnesota-Twin Cities, Minneapolis, MN

The Concussion Executive Committee© (derived from the Ice Hockey Summit II: Action on Concussion committees (2015)). All rights reserved. The CEC has granted the publisher permission for the reproduction of this article.

Address for correspondence: Michael J. Stuart, MD, Mayo Clinic Sports Medicine Center, 200 First Street SW, Rochester, MN 55905, e-mail: stuart.michael@mayo.edu.

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Introduction

Ice hockey, a game with inherent risks of injury, is played in North America and Europe at high speeds, on hard ice, with boards, sticks, and pucks (1). Ice hockey, played primarily in regions frozen for over 6 months of the year, also can bring joy when played in a fun and respectful yet competitive manner. Collisions, body checking, and illegal on-ice activity results in potentially serious consequences including sport-related concussions (SRC)/mild traumatic brain injury (mTBI) (2–5). These proceedings disseminate information presented at Ice Hockey Summit II: Action on Concussion in context with accomplishments made since Summit I, 2010. Action items from the five sectors identified for Summit II, 2013, were voted on and prioritized in five areas: 1) Basic Science of Concussions in Ice Hockey: Taking Science Forward, 2) Acute and Chronic Concussion Care-Let’s Make a Difference, 3) Preventing Concussions (Behaviors, Rules, Education and Epidemiology): Measuring Effectiveness; 4) Updates in Novel Equipment (Helmets, Chin Straps, Mouth Guards): Their Relationship to ASTM, ISO, and BNQ Standards, and 5) Policies and Plans for Organizations: State, National, and Federal Levels. The evidence-informed support for each of the sectors is discussed from the perspective of published literature, action accomplished since 2010 and compelling new science (6,7). To update Summit II attendees, the status of action items prioritized during Summit I were summarized briefly and reported in the following paragraphs.

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Databases and Metrics

Little progress occurred since Summit I in certifying health care professionals who have SRC expertise or in establishing stringent concussion metrics, databases, or a national concussion registry (7–10). All states have accepted a version of the Lystedt Law, which dictates that RTP is the job of a licensed health care provider; however there is no centralized registry to document concussion information. Injury reporting surveillance programs through the National Collegiate Athletic Association, the National Athletic Treatment, Injury, and Outcomes Network, and the Reporting Information Online system collect epidemiological injury and concussion data across multiple sports at collegiate and high school levels. However, these databases are not hockey specific; they lack a consistent concussion definition, and data collected are not concussion specific. In the absence of a national injury registry, these resources allow us to measure SRC better across sports and age groups using more standard methods so that trends over time can be detected (11).

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Recognizing, Diagnosis, Management, and Return to Play

Criteria for recognition, diagnosis, and return to play (RTP) of athletes with SRC are evolving. SRC is accepted as a brain injury that in 80% to 85% of athletes resolves within 10 d (6,7). Traditional neuroimaging (computerized tomography (CT) and magnetic resonance imaging (MRI)) is usually normal. Advanced imaging such as functional MRI (fMRI) or diffusion tensor imaging (DTI) may identify SRC in research studies, but these techniques are not generally suitable for direct clinical use (12). “No same day RTP” and RTP, only after symptom resolution, are clearly now responsibilities of licensed health care professionals (13).

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Player Equipment and Facilities

Hockey helmet standards and designs have not changed since Summit I. Helmets effectively mitigate impact energy but do not prevent SRC, and no scientific evidence confirms the preventive effect of mouth guards in reducing SRC. Helmet testing standards are based on biomechanical thresholds for skull fracture and severe TBI — not concussion (mTBI). Tolerance limits for SRC have been proposed, and sensors detecting head acceleration are studied in relation to symptom onset and concussion diagnosis (14,15). Debate continues within standard organizations about how acceleration tolerances can be implemented in helmet testing and whether SRC risk can be reduced by helmet design. Hockey helmets and mouth guards are worn in a manner noncompliant with manufacturers’ instructions, thereby impeding the in vivo assessment of helmet effectiveness (16,17).

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Education and Prevention

Hockey requires behavior modification to reduce SRC. Fair Play (FP), a component of the Minnesota Hockey Education Program, was implemented 10 years ago, a result of collaboration with Mayo Clinic. Game score sheets, analyzed annually by Mayo Clinic Sports Medicine, track major infractions such as head hits and checking from behind (CFB). Tougher sanctions are imposed as needed to influence these behaviors. “Heads Up, Don’t Duck,” Play it Cool (PIC) (Coaching Education), ThinkFirst Smart Hockey, and Concussions and Female Athletes: The Untold Story, viewed more than 2,500 times, increase SRC awareness (18–21). Education of coaches, parents and players in conjunction with a behavioral modification program have the potential to help decrease SRC in hockey (22).

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Rule Changes, Policies, and Enforcement

Pee Wee hockey leagues (ages 11 to 12 years) that allow body checking increase the risk of SRC three-fold compared with leagues without body checking (23). USA Hockey championed a rule change in 2011 that prohibited body checking in Pee Wee games but allowed checking skills to be taught during practices. The rationale to delay checking in games until Bantam (age 13 to 14 years) hockey was based on studies that document decreased risk of concussion (23,24) and the premise that skill development may progress faster without checking. Furthermore, evidence supports more positive game outcomes based on win-loss-tie record in teams with fewer injuries through the season (25) and significant reduction in health care utilization costs in leagues where body checking is not allowed (26). A body checking discussion meeting in 2014 (27) included a task force of researchers and community partners from Canada and the United States. The deliberations led to an evidence-informed decision to delay body checking until age 13 years (Bantam) (24,25,27,28). Minnesota data showed fewer checks from behind and head hits in the United States after the rule change. Data based on the rule change regarding SRC incidence, economics, player attrition, and skill development in hockey will be available in the future.

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Communications

Seven journal editors simultaneously published the post-Summit I Proceedings, and television news casts disseminated our concerns about the need for a rule change. Increasing awareness helped obtain affirmative vote. Other media-based communications occurred before, during, and after Summit I. Jeff Klein, New York Times, wrote extensively (29,30), Ken Dryden published on the Summit and concussion, and other newspapers carried Summit-related SRC articles.

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Summit II: Action on Concussion

In the United States, more than 300,000 SRC occur annually across all sports at all levels of competition (12,31–33). Ice hockey SRC prevalence is high, and reducing SRC requires the collaboration of medicine, epidemiology, psychology, sport science, coaching, engineering, officiating, manufacturing, and our community partners. Hockey players compete at high speeds as they mature, risking injury from intentional and accidental collisions, body checks, illegal on-ice activity, and fighting. These behaviors may result in SRC, possibly accompanied by brain microstructure alterations and occasionally a catastrophic brain or spinal injury (5,34–36). The following case study of a hockey player relates to the concussion science that was presented during Summit II.

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Concussion in a Professional Hockey Player

JM, age 27, with two previous concussions, sustained a blow to the head with no loss of consciousness but fell skating off ice. CT and MRI findings were negative, but exercise exacerbated his SRC symptoms. Four months later, after gradual rehabilitation, he returned to hockey. After five games, an elbow to his chin resulted in JM’s head striking the glass. Cognitive and physical rest, chiropractic manipulation, and massage provided temporary relief, but headache, fatigue, irritability, anxiety, dizziness, and forgetfulness remained. Depression and anxiety symptoms were abnormally high, despite normal neuropsychological (NP) examination results. His activity progressed as his symptoms resolved. After returning to the NHL, he was checked headfirst into the glass and, despite dizziness, finished the game. After weeks of rest, his postconcussion symptom score was 72 due to blurry vision, headache, anxiety, irritability, sleep disturbance, and fogginess. His multidisciplinary concussion care team utilized advanced imaging, physical and chiropractic therapy, vestibular rehabilitation, pharmacology, cognitive and behavioral rehabilitation, and psychiatric interventions. His anxiety and depression did not resolve and prompted a recommendation that he retire from professional hockey. He then faced the challenges of transitioning from a professional hockey career and coping with loss of exercise, travel, prestige, excitement, quality sleep, and teammate camaraderie.

Before discussing the science of concussion in depth, the idea that all SRC cannot be prevented was reiterated. SRC reduction in a collision sport must address modifiable extrinsic and intrinsic risk factors. Prevention protocols should include a strict definition of SRC with valid markers of severity based on prospective studies with sufficient power in specified populations, which incorporate individual exposure time (IET) (6–10,14,37–42). Evaluations should be provided by qualified health care providers at point of care (9). Learning the mechanism of head trauma (e.g., video review) and using multivariate analysis to adjust for covariates and control for clustering also are important (43).

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Section 1: Basic Science of Concussions in Ice Hockey: Taking Science Forward

Macro Trauma

High school, collegiate, and junior A hockey teams (n = 11) wore instrumented (HITS) helmets between 2006 and 2013 and >100,000 head impacts were recorded. Male and female players experienced 2.9 ± 1.2 and 1.7 ± 0.7 head impacts, respectively, per practice or game to the front (30%) and back (33%) (44–49). Player-to-player contact accounted for 50% of head impacts in both male and female leagues, followed by contact with boards and ice; males sustained higher linear and angular accelerations. The largest accelerations resulted from head contact with ice. Head impact exposure (HIE) — frequency, magnitude, and head impact location — correlated with signs, symptoms, and neuroimaging (fMRI with DTI) of diagnosed concussions in high school, collegiate, and professional hockey and football players. HIE differed significantly for immediate versus that for delayed presentations of SRC (50,51). More SRC in hockey were diagnosed on days with higher numbers of impacts and greater impact magnitudes than those on days with fewer impacts and lower magnitudes.

An in-depth investigation of junior A players measured SRC history, SRC diagnosed in season, HITS accelerations, IET, penalties, video data, and on-ice behavior predisposing to concussion. HITS recorded 5,201 impacts over 10 g in 2011 to 2012 and 2,780 impacts in 2012 to 2013. Impact frequency, between 102.9 and 185.8 per player per season, averaged 7.06 impacts per game in season 1 and 6.82 in season 2. Eight SRC were diagnosed in 2011 to 2012 and four in 2012 to 2013. Thirty-four fighting penalties were called in season 1 and 49 in season 2. Video analysis of behavior conducive to SRC included skating with the head down, negative body position (i.e., no anticipation or body awareness) and fighting (52). This research provided accelerations and footage for video reconstruction input for finite element modeling (FEM) (53) to determine strain and strain rate inputs for stretching in a rat neuron model.

Video reconstruction determines the relationship between head impacts and hockey SRC, manifested by the dynamic response and brain tissue deformation calculations. A validated FEM of the skull and brain is used to obtain objective data (36). SRC impact videos reconstructed at the Neurotrauma Impact Science Laboratory (NISL), Ottawa, Ontario, Canada, were obtained via collaboration with coinvestigators or via an Internet search. Impacts with multiple lines and circles visible in a wide camera view, a close-up of impact location, head contact from a striking player, using a shoulder or elbow, and a victim who did not strike his head again are eligible for use. Impact velocity requires establishing the distance separating a striking player’s elbow or shoulder and the struck player’s head five frames before impact (34,35,54–56). The lines and circles provide a scale reference to convert pixels to meters (±5% accuracy), and a reference grid determines impact location (57,58). This system creates rectangular targets more precisely than previous reconstructions. Impact direction uses increments of 30°. Variation of 30° for a side impact matters little when recreating a shoulder-to-helmeted head hit in hockey. This method replicated a previous study of skilled players striking a Hybrid III head form using four techniques identified from hockey videos. Shoulder impacts used a high-mass, high-compliance surrogate, while elbow impacts used a low-mass, low-compliance surrogate. Both surrogates generated similar linear acceleration, peak curve length, and brain deformation as those generated by players. Recent data from NISL showed that a punch in hockey generates greater magnitude of angular acceleration than collisions with the ice, a shoulder, or the puck, supporting the need for rules to curtail fighting in hockey (59). Understanding macro trauma prompts the question of how the brain responds at a cellular level.

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Micro Trauma

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In vivo

An in vivo postconcussion rodent model was used to study concussion, repeat concussion, and postconcussion cognitive impairment and intervention effect on behavior. mTBI in rodents is induced by fluid percussion, weight drop, and closed head injury. Experimental mTBI induces a neurometabolic cascade (NMC) that includes ionic flux, indiscriminate glutamate release, energy crisis/mitochondrial dysfunction, axonal injury, and alterations in neurotransmission (60–63). Behaviors studied after TBI included working memory (WM), spatial learning and memory (SL&M), fear-based learning, motor coordination, and depression. WM (retaining short-term information for manipulation), disturbed after mTBI, was measured in rats using a novel object recognition (NOR) test. Impaired NOR recovered 7 to 10 d after mTBI. WM was worse after repeat mTBI than that after a single mTBI. SL&M tested using the Morris Water Maze (MWM), showed mTBI disturbed MWM learning in juvenile rats, and SL&M deficits worsened after repeat mTBI (64). mTBI combined with fearful stimulus enhanced fear response, which may persist, as in posttraumatic stress disorder (65). Animal models enable timing control of post-mTBI insults to identify a vulnerability window for repeat mTBI or exercise. Post-mTBI energy crisis persists 3 to 14 d and was injury model dependent. Repeated mTBI during an energy crisis period causes more severe, prolonged metabolic and memory impairments (66). Early post-mTBI exercise interferes with nerve growth factors and cognitive recovery, but after the acute phase, exercise facilitates recovery (67).

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In vitro

Before treating SRC in vivo, cellular pathways leading to clinical complications must be understood. Head acceleration and brain deformation during collisions correlate with SRC. Hypotheses for how mechanical forces translate to cellular neural dysfunction include strain-induced membrane poration, ion channel dysfunction, and integrin stimulation-induced Rho-ROCK signaling (68,69). In these SRC studies, whole-body macroscopic forces sensed at a cellular level are transduced pathologically. No one pathway has been identified, and each mechanism may play a role. The SRC mechanism may depend on mechanical load on the brain cells. To determine SRC mechanisms, in vitro experimental models must be developed with physiological structure and function, as connecting collision forces to neuronal injury is difficult and costly using in vivo animal models. Microfabricated biological systems have advanced to organ-on-a-chip technology, so in vivo function can be reproduced in microscale in vitro systems and used to study biological mechanisms or utilized as high-throughput pharmaceutical test beds (70–74). This technology permits probing all stresses and strains to which neurons are exposed in SRC to determine the level at which brain deformation causes dysfunction. There have been only a few neurotrauma organ-on-a-chip studies, but the basic science of SRC will advance rapidly as brain-on-a-chip technology evolves.

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Section 2: Acute and Chronic Concussion Care: Emphasizing Diagnosis, Evaluation, and Concussion Consequences

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Medical Diagnosis of SRC

A neurologist describing the science of SRC acknowledged that cell ion channel dysfunction and awareness of potential pharmacology intervention sites in SRC have evolved. Increased extracellular potassium and glutamate, activation of N-methyl-D-aspartate receptors, neuron depolarization, and glial activation depicting the postconcussion NMC may result in cortical spreading depression (CSD). After SRC, CSD leads to inflammatory cascade from neuronal Pannexin1 (Panx1) megachannel opening, caspase-1 activation, release of high-mobility group box 1 (HMGB1) from neurons, nuclear factor κB (NFκB) activation in astrocytes, and release of prostanoids and cytokines such as IL-1β and TNF-α (75). This cascade may be disrupted by inhibitors of Panx1 channels (e.g., probenecid), NFκB (e.g., aspirin, feverfew), or inhibition of prostanoids (nonsteroidal anti-inflammatory drugs). The post-SRC NMC and upregulation of aquaporin (water channel) proteins in astrocyte plasma membranes are partially responsible for brain edema after SRC. Intranasal nerve growth factor, given after mTBI, reduced brain edema in an animal model by inhibiting the transcription and expression of IL-1β, TNF-α, NFκB, and aquaporin channel expression (76). SRC and CSD are associated with intercellular calcium (Ca++) waves that spread through astrocyte networks. Ca++ wave propagation after SRC is mediated partly by purinergic receptors. Antagonism of purinergic receptors reduces neuron death and improved histological and cognitive outcomes in a TBI animal model. While most mTBI interventions involve animals, a recent double-blind placebo-controlled clinical trial in warfighters with concussion evaluated N-acetylcysteine (NAC), an agent with antioxidant and anti-inflammatory properties (77). Warfighters given NAC within 25 h of blast induced mild traumatic brain injury (bTBI) had fewer symptoms compared with those receiving placebo, demonstrating effective short-term treatment for bTBI. This work was replicated subsequently in rodents (78). The benefit of early intervention impeded the post-bTBI NMC; however larger confirmatory studies are mandatory after SRC.

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Imaging SRC (mTBI)

Although CT neuroimaging for acute, moderate, and severe neurological trauma demonstrates hemorrhagic intracranial lesions, changes from mTBI injury are rarely apparent. Occasionally T2 and T2* MRI detects lesions not seen on CT imaging. fMRI demonstrates disruption of neuronal network activity after mTBI (79). Increased functional activity after head trauma shows that higher level of brain activation is required to perform memory tasks compared with controls (80). Specific brain biomarkers detected with advanced MRI techniques and fMRI with DTI can elucidate the intracellular impact of mTBI (81–83). MR spectroscopy offers a quantitative measurement of brain injury. N-acetylaspartic acid (NAA) decreases in the presence of trauma, and NAA/creatine ratios have been proposed to measure mTBI severity and monitor recovery (84).

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NP Testing in SRC

Division 1 football and hockey players wore HITS helmets (n = 214) to assess the effect of a season of head impact on cognitive performance compared with a noncontact athlete control group (n = 45). Using ImPACT™ (85) and seven measures from an NP test on contact (n = 55) and noncontact athletes (n = 45), few cognitive differences were detected before or after season assessments. More contact athletes performed more poorly than predicted postseason on new learning (CVLT) compared with noncontact athletes (24% vs 3.6%; P < 0.006), suggesting that repetitive head impacts may impede learning. Although contact athletes, veterans of several seasons, tested once showed no impaired cognitive function; 8% to 12% of veteran hockey players scored >1.5 SD below baseline on several NP tests. Players (n = 11) who sustained SRC during the season tested 1 to 3 d after SRC showed loss of practice effect, performance declines, and increased symptoms compared with nonconcussed and noncontact athletes. The concussion symptom profile was statistically significant in this small sample. On the Stroop interference test, 50% of players with concussion scored >1.5 SD lower than predicted, based on preseason performance. Data suggest immediate SRC effects on cognition but no lasting cognitive effects in players with repetitive, subconcussive head trauma during one season (46).

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RTP Conditioning Treatment for SRC

Evaluation and treatment must be based on SRC physiology. Exercise testing to the level required in sport, after SRC without symptom exacerbation, defines recovery (12). The Buffalo Concussion Treadmill Test (BCTT), based on the Balke cardiac treadmill protocol, diagnoses SRC physiological dysfunction, differentiates it from a diagnosis of cervical injury, quantifies severity, and determines exercise capacity (86–91). When athletes with SRC achieve maximum exertion and are at baseline or normative level of symptoms, they are physiologically ready to begin the monitored Zurich RTP protocol. Athletes with SRC who demonstrate submaximal symptom-limited threshold on the BCTT have not recovered. For athletes not recovered, aerobic exercise (AE) at a subthreshold target heart rate (HR), which is 80% to 90% of the HR achieved on the BCTT, 20 min·d−1, accelerates safe recovery (88,91). Athletes are instructed to exercise aerobically at target HR using an HR monitor to stay below symptom threshold. Target HR can be increased by 5 to 10 bpm every 1 to 2 wk depending on individual recovery rate. Athletes are recovered physiologically when they can exercise at their usual perceived exertion for competition for 20 min without symptom exacerbation. SRC athletes may have visual or vestibular signs and symptoms that do not resolve with progressive AE that require treatment. Nevertheless they should continue AE to improve mood and fitness. A recent study showed that the BCTT helped establish physiological recovery in accordance with the Zurich RTP guidelines and was 100% successful at returning SRC adolescent athletes to sport (93). Provocative exercise testing is consistent with expert consensus opinion on establishing physiological recovery from SRC (12).

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Persistent Postconcussion Cervical/Vestibular Concerns

Dizziness, neck pain, and headaches are SRC symptoms frequently reported in hockey players (9), including youth (93). There is paucity of literature evaluating treatment in individuals with persistent symptoms after SRC (94). Reportedly the cervical spine is a source of cervicogenic headaches and posttraumatic cervical spine pain (95). Dizziness after trauma has been attributed to vestibular and cervical dysfunction (96). Persistent dizziness, neck pain, and headaches, attributed to cervical spine and vestibular system involvement, may be amenable to cervical spine and balance treatments. Functional and symptomatic improvements in individuals with persistent dizziness after SRC have been observed following a course of vestibular rehabilitation (97). Combined manual therapy and exercise for the cervical spine is a widely accepted treatment for individuals with cervical spine pain and cervicogenic headaches (98,99). Recent evidence has demonstrated significant treatment effects in individuals with persistent symptoms of dizziness, neck pain, and headaches following SRC, who were treated with a combination of cervical and vestibular physiotherapy techniques (100).

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Concussions in Females, Youth, and Players with Emotional and Behavioral Disorders

Studies of SRC in hockey may neglect populations such as females, youth players, and those with emotional and behavioral disorders (EBD) (19,101–105). Although females have lower rates and frequencies of SRC than males when collapsed across sports and ages, SRC in college hockey is higher for females but there is greater severity in males. SRC is the most common hockey injury for both genders, but genders report symptoms differently, perhaps due to differences in sensitivity, physiological parameters, and reporting styles (103). SRC risk in youth players is unknown. Although SRC rates are lower in high school than those in college, SRC incidence is higher in youth players. SRC in hockey may be more frequent among youth than adult players. Cognitive impairment in youth lasts longer than that in adult athletes, and extended RTP protocols may be required compared with players over age 18. Second-impact syndrome, or diffuse cerebral swelling after mTBI, occurs most often in youth (104). Preexisting EBD (e.g., depression and anxiety) influence post-SRC adjustment and recovery after SRC symptoms mimic and exacerbate preexisting depression and anxiety, thus influencing postconcussion syndrome. Premorbid attention deficit hyperactivity disorder exacerbates post-SRC symptoms. Adjustment difficulties, irritability, aggression, and trouble concentrating are inherent in ADHD and are also characteristic of post-SRC (101).

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Genetic and Epigenetic Implications for SRC

The genome, epigenome, structure, and brain function are being studied using neuroimaging and neuropsychometric measures to determine whether specific athletes are at risk for SRC. Genetic and epigenetics (environmental influences) affect human traits. Investigators can determine whether 1) genes contribute to a trait and 2) environmental factors (i.e., adversity and trauma) modify traits: a “gene by environment” approach. Of 1,676 adolescent twins, 13.3% reported mTBI. Concussion was not influenced genetically, but attention problems (P < 0.005), aggressive behavior (P < 0.05), somatic complaints (P < 0.005), and thought problems (P < 0.01) were influential (106). Apolipoprotein E (APOE), brain-derived neurotrophic factor (BDNF), and Tau are associated with mTBI risk or prolonged recovery (107,108). BDNF influences cell growth, differentiation, and neuronal survival. Certain tau genotypes have been associated with self-reported concussions (109). Tau proteins belong to the microtubule-associated protein family. Microtubule components of axons influence cell shape and protein, hormone, enzyme, and neurotransmitter transport along axons (110). SRC studies should include genetic, epigenetic, neuroimaging, and phenotype collected at baseline, after SRC, and after season.

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A Pathophysiological View of Head Trauma Effects

Chronic traumatic encephalopathy (CTE), a progressive neurodegenerative disease, has been associated with repetitive TBI in collision sports and warfighters (111–114); however association is not causation. CTE is manifested by symptoms that occur after latency periods of years to decades. The insidious onset of irritability, impulsivity, aggression, depression, suicidality, and short-term memory loss progresses to include cognitive deficits and dementia. CTE, characterized by hyperphosphorylated tau protein in neurons and astrocytes, is in a pattern distinct from other tauopathies, including Alzheimer’s disease. Hyperphosphorylated tau starts as perivascular neurofibrillary tangles and neurites deep in cerebral sulci, spreads to adjacent superficial layers of cortex, and spreads to involve medial-temporal lobe structures, diencephalon, and brainstem. Over 85% of CTE cases show accumulated phosphorylated 43 kDa TAR DNA binding protein (TDP-43) in addition to abnormal aggregations of hyperphosphorylated tau. Macroscopic changes in advanced CTE include cavum septum pellucidum, septal fenestrations or septal absence, diffuse brain volume reduction in frontal, temporal, and medial temporal lobes, hypothalamus, medial thalamus, and mammillary bodies, and ventricular enlargement with disproportionate dilatation of the third ventricle. Currently CTE can be diagnosed only after death; thus its incidence and prevalence are unknown. Objective, validated biomarker(s) are essential to determine CTE risk to athletes. Noninvasive diagnostic techniques include MRI, DTI, magnetic resonance spectroscopy, and positron emission tomography (PET) using ligands specific for paired helical filament tau (115,116). These potential consequences of concussion are of concern to the medical community and general public; prevention is key.

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Section 3: Preventing Concussions via Behavior, Rules, and Education

Perspectives of a Clinician, Investigator, and Minnesota State High School League Sports Medicine Chair

Most injury reduction policies are not evidence based. Reducing SRC prevalence and severity includes reducing collisions, rule enforcement, and raising awareness about equipment strengths and weaknesses (i.e., helmets, face shields, and mouth guards). Primary SRC-specific strategies include reducing collisions by prohibiting body checking, rule enforcement aimed at elimination of head contact, increasing rink size or reducing the players on ice, and increased punishment to deter dangerous infractions. Secondary SRC reduction strategies, actions that require behavioral changes to promote safety, require culture changes across constituents, strict rule enforcement, targeted education programs, and FP. When higher injury and SRC rates were reported in a community hockey cohort and a prospective tournament cohort, due to collision and body checking, delaying body checking age to decrease injuries was recommended (102). A decade later, an age-matched larger cohort of youth players in a body checking league were compared with a non-body checking league (2010) (25). Three times more injuries and four times more concussions in a Pee Wee (ages 11 to 12 years) body checking league prompted a policy change by USA Hockey in 2011, replicated in 2014 by Hockey Canada. Body checking skills are taught in Pee Wee but not allowed in games until Bantam (ages 13 to 14 years). SRC, often due to rule infractions, mandates rule compliance. Educating all hockey stakeholders is critical to player respect. Player attitudes showed that 32% would check illegally and 6% would injure another player to win. Hockey is safest during practices and in non-body checking games (105). Behavior modification programs, such as FP, can shape player, parent, and coach attitudes, and combined with strict rule compliance and enforcement, are critical in our attempts to achieve player safety (16,117).

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Preventing Concussions by Education and Behavioral Modification (FP)

Games governed by FP rules can decrease major penalties and game-related injuries, such as SRC (16,117). SRC consequences have resulted in modest financial support for behavioral modification programs, such as FP, and educational programs, such as Respect and Protect, Safety Clinics, Smart Hockey (Think First Foundation), (20) and PIC, an online coaching education program (21). FP, an evidence-based program, launched in Minnesota in 2004, rewards sportsmanship and penalizes dangerous on-ice behavior. In Minnesota hockey, score sheets depict major and minor penalties and if FP points were earned or lost. Pee Wee players, in 2004 to 2005, averaged 28 CFB penalties per 100 games. In 2011 to 2012, after implementation of no checking in games, Pee Wees achieved an 8-year low of only 3 CFB per 100 games. Head contact also decreased from over 12 per 100 games to less than 1 per 100 games (118). Despite FP point calculations, not all coaches, parents, and players are aware of their teams’ FP standings. There is no SRC registry to gauge the influence of FP on decreasing concussions statewide and <25% of directors voluntarily run their tournaments by FP. Measuring FP effect in junior A tournaments (16) or across a single season (117) or decade (SMC) at specific levels of participation has demonstrated effectiveness in decreasing head hits (118). In 2013 to 2014, USA Hockey funded a study to determine whether players in tournaments governed by Intensified FP (IFP) sustained fewer SRC and major penalties and provided players equitable on-ice time and whether IFP teams earned more FP points than teams in non-IFP tournaments. While data are being analyzed, next steps include initiating a hockey SRC registry in Minnesota, implementing the team Safety Parent, making FP mandatory in all tournaments, and ensuring FP points influence regular season and tournament outcomes.

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PIC: A Safe Hockey Coaching Education Program

The PIC Safe Hockey Program was designed to enhance the ability of coaches to teach skills with emphasis on safety using a structured, facilitated, online curriculum that can be delivered asynchronously. The PIC program consists of three modules that focus on strong skating skills, on-ice awareness, and risk management from an injury prevention perspective. Evaluation of the PIC program found that although there were no significant differences in the number of observable positive behaviors between PIC and non-PIC teams, there was a higher number of negative behaviors observed among non-PIC team players at every level of participation (Atoms, Peewee, and Midget) (21). Concussion occurrence has not been evaluated.

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A Scientist and Hockey Coach’s View of Concussion Prevention

SRC science can be daunting for coaches. The coaches’ role in injury prevention is to teach children age-appropriate hockey fundamentals and foster an environment of sportsmanship. Introducing the skills to deliver and receive a body check safely can result in safer hockey (16,25). For example, anticipating collisions (119) and delivering legal body checks may reduce head impact severity. Engaging hockey players in high-tempo and game-related drills helps prepare players for unexpected collisions sustained in games. “Small ice” drills require that players pass, shoot, and body check in small confined spaces (i.e., corner of the rink) and teaches them “heads up” and “do not look down.” These skills help players anticipate collisions and prepare for opposing player infractions. Our investigative team identified that >17% of body collisions reviewed on video were USA Hockey rule infractions (29). Of those, 67% resulted from intentional head contact with elbows, sticks, or bodies. Brust et al. reported that 15% of injuries were intentional and 34% of injuries occurred in games characterized as “hostile” (16). Players must be taught to respect and not injure opponents. Coaches and officials must ensure that players are taught to play fairly in compliance with the rules. Scientific research combined with basic instructional fundamentals can provide the basis for rule changes to protect players from unnecessary head trauma, such as SRC.

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Summary

At the conclusion of the presentations and breakout sessions, four to five strategies that emanated from each breakout were projected on slides and attendees were asked to prioritize these using the Audience Response System. The following action items shown in the blocks of the figure were deemed most important to decrease SRC in ice hockey (Figure).

Figure. Ac

Figure. Ac

The information from this summit provided solid support for and placed its strongest emphasis on removing all head hits and fighting from the game. This highly prioritized action item already has been initiated by USA Hockey rule changes:

Tier 1 and 2 Junior A: A major penalty plus a misconduct penalty shall be assessed to any player who engages in fighting. A minor, double-minor, or major penalty plus a misconduct penalty, at the discretion of the referee, shall be assessed to any player who, having been struck, continues the altercation by retaliating.

Tier 3 Junior A: A major penalty plus a game ejection penalty shall be assessed to any player who engages in fighting. A minor, double-minor, or major penalty plus a game ejection penalty, at the discretion of the referee, shall be assessed to any player who, having been struck, continues the altercation by retaliating.

Additional Summit II priorities include the following: 1) designing studies that implement rigorous research epidemiology, 2) moving to standardizing an objective concussion assessment compatible with established diagnostic criteria, and 3) certifying those players eligible to return to hockey. Preventive measures also were deemed critical, such as increased coaching education, wearing equipment in compliance with manufacturer instructions, and making changes to rules, policies, and the overall hockey culture.

When these highly prioritized actions are carried out, SRC in ice hockey will decrease and the action plan will be viewed as success.

“Science has responded to the game on the ice. Now it’s up to the game on the ice to respond to the science.”

Ken Dryden, October 2013

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Acknowledgments

The authors thank Carol Best, Casey Twardowski, John Hollman, Sharanne Calabrese, Kurt Requa, Jason Ward, Nichelle (Nicki) Smith, and Janelle Jorgensen.

Additionally two brief presentations preceded the official Summit II program. We thank Dr. Miranda Lim for presenting her work on sleep disturbances after mTBI and Drs. Don Weaver and Ryan D’Arcy for presenting on a new quantitative electroencephalogram device measuring brain activity after head trauma. Studies on these topics show promise for diagnosis and treatment of SRC and are a point of departure for clinical research.

The supporting organizations are Brian Mark Family Fund, USA Hockey, International Ice Hockey Federation, Hockey Equipment Certification Council, and Ontario Neurotrauma Foundation.

Manuscript style was retained based on permission to reprint.

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